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Systematics, Ecology, and Application of Helotiales

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Systematics, Ecology, and Application of Helotiales Mycoscience VOL.62 (2021) 1-9 Review Systematics, ecology, and application of Helotiales: Recent progress and future perspectives for research with special emphasis on activities within Japan Tsuyoshi Hosoya National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba-shi, Ibaraki, 305-0005, Japan ABSTRACT Helotiales is one of the most diverse groups of apothecial ascomycetes, including 3000–4000 taxa. Recent progress in the systematics, ecology, and their applications through research is herein reviewed based on the experiences of the author with a special emphasis on activities in Japan. In the past 30 y, more than 50 helotialean taxa have been added to the mycobiota of Japan, including new taxa. With the advent of molecular phylogeny, some families have been revisited, such as members with stroma (Sclerotiniaceae and Rutstroemiace- ae) or hairs (Hyaloscyphaceae and Lachnaceae). Although the monophyly of Helotiales has not yet been demonstrated, our understand- ing of its phylogeny has greatly advanced. The unexpected ecological nature represented by endophytism has been revealed through barcoding and other molecular techniques. The research history of ash dieback is also reviewed, and the endophytism/saprophytism of the pathogen on its original host is discussed. Drug discoveries within Helotiales are reviewed, and successful examples are presented. As future perspectives, both the cumulation of occurrence and sequence data of Helotiales is greatly encouraged to elucidate this important group of fungi. Keywords: discovery research, Hyaloscyphaceae, Lachnaceae, Rutstroemiaceae, taxonomy Article history: Received 5 March 2020, Revised 12 May 2020, Accepted 13 May 2020, Available online 20 January 2021. 1. Introduction high level of species diversity, which may be reflected in their met- abolic diversity, but relatively underexplored not only taxonomical- Among the apothecial ascomycetes with inoperculate asci, Hel- ly but also in applied science. 4) They are also thought to be ecolog- otiales is one of the most diverse groups. It is known to include ically diverse, suggesting diverse metabolites. In short, Helotiales some 3000–4000 taxa (Kirk, Cannon, Minter, & Stalpers, 2008; are underutilized but easily accessible fungi (Hosoya, 1998). Baral, 2016). Most members of the Helotiales have minute apothe- I have been working on this attractive group of fungi for more cia, usually less than 2 mm diam. They may be sessile or stipitate, than 30 y, first as a researcher in the private sector in search of nov- dark to bright colored, and superficial or erumpent through the el biological resources for metabolites, and then in a more pure sci- plant host. The overall shape of the apothecia is cupulate-discoid, ence-directed position. Through my career, I have made many new turbinate funnel-shaped, or clavate (Korf, 1973). Most are known to discoveries and contributions to the field of systematics and discov- be saprophytic, living on fallen leaves and decaying wood, but some ery research. In the present article, I review recent advances and are parasitic to pathogenic or symbiotic with other organisms. future perspectives for research on this attractive group of fungi. Many members are relatively easy to isolate, but the inducing the formation of apothecia in vitro is not easy (Müller & Loeffler, 1976). 2. Systematics Though not frequent, some members produce an asexual state, but many remain unassociated with this state. Despite these biological 2.1. Infrastructure for systematics diversities, taxonomy and ecological studies are insufficient. From the viewpoint of applied science, in particular discovery Collecting specimens is a fundamental of systematics. In the “in research, Helotiales are an attractive biological resource for the fol- situ” activity in the National Museum of Nature and Science, the lowing reasons. 1) They are in different ecological groups than soil following process is usually applied. Once the specimens are col- fungi. 2) Most are easily accessible and culturable. 3) They have a lected, single spore isolation using Skerman’s manipulator (Sker- man, 1968) or multisporous isolation from discharged ascospores is * Corresponding author. attempted, then the specimens are heat dried or air dried and E-mail address: [email protected] (T. Hosoya) stored as voucher specimens in the fungarium. DNA is extracted This is an open-access paper distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivative 4.0 international license (CC BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.47371/mycosci.2020.05.002 ― 1 ― 01_CW6_AX440D01.indd 1 2021/01/08 11:44:15 T. Hosoya / Mycoscience VOL.62 (2021) 1-9 Ex situ In situ Other collections Field （Personal, Abandoned） Collecting Acception Materials Processing (format, databasing) Isolation, Cultivation DNA / tissue samples Specimens Isolates Fungarium External Culture Collection Deep freezers NITE-NBRC, JCM, etc. Figure 1. Diagrammatic representation showing the research process and management of voucher specimens. from the isolates and stored in a freezer as a sample for future use. 1996), and it is now known as a separate group (Orbiliomycetes) When isolation is not successful, part of the apothecia is kept in a from Helotiales and is recognized as a primitive member of the buffer [20% DMSO, 100 mM Tris-HCl (pH8.0), 250 mM EDTA, 100 apothecial fungi (Eriksson, Baral, Currah, Hansen, & Kurtzman, mM Na2SO3, NaCl to saturation; Hosaka & Castellano, 2008] for 2003; James et al., 2006). Studies are largely limited to Dermateace- DNA extraction when necessary. If asexual reproduction is recog- ae, Hemiphacidiaceae, and Leotiaceae. In my previous studies, I nized in culture, the culture of isolates may also be dried and regis- worked with Hyaloscyphaceae and Sclerotiniaceae sensu lato, tered as specimens. Because our facility is not suitable for the which are reviewed below. maintenance of cultures, we have a close collaboration with cul- ture collection facilities that have the capacity to store intriguing 2.3. Taxonomy of Hyaloscyphaceae isolates from the specimens (Fig. 1). Given the above process, four major collections (specimens, Hyaloscyphaceae is a large family (74 genera + 61 synonyms, isolates, extracted DNA and tissue samples) were obtained and 933 species., Kirk et al., 2008), composed of fungi with minute to managed in-house (http://db.kahaku.go.jp/webmuseum_en/; da- small apothecia with various hairs. The generic taxonomy of these tabase opened for specimens only) or ex-house (e.g., NBRC, https:// fungi was based on a combination of characters, including that of www.nite.go.jp/nbrc/catalogue/NBRCDispSearchServlet? hairs, ectal excipular structure, and paraphyses. Korf (1973) subdi- lang=en; GBIF, Global Biodiversity Information Facility, https:// vided the family into two subfamilies: Trichoscyphelloideae, includ- www.gbif.org/) databases. These collections may be linked with ing a single genus, Lachnellula, and subfamily Hyaloscyphoideae. sequence data on publicly accessible databases (INSDC, http:// The latter was subdivided into five tribes (Arachnopezizeae, Hyalos- www.insdc.org/). All of these sites were visited on Feb 25, 2020. cypheae, Lachneae, Trichodisceae, and Trichopezizelleae). Most The occurrence data based on the specimens were also provided to members of Hyaloscyphaceae belong to Arachnopezizeae, Hyaloscy- GBIF for global use. Our systematic studies were based on these pheae, Lachneae, and Trichopezizelleae. A number of genera with infrastructures. similar morphology have been identified in Lachnum, one of the major genera in Lachneae, and even more genera have been pro- 2.2. Advances in the systematics of Helotiales and their stud- posed (e.g., Baral & Kiriegelsteiner, 1985). However, because mor- ies in Japan phological characters often show convergence, revision of generic taxonomy based on phylogeny is warranted. Korf (1973) published a key to the genera of Helotiales with tax- Otani (1989) summarized the known occurrence in Japan and onomic comments. This monumental publication covered a wide listed 41 taxa. However, we expected more undocumented mem- range of taxonomic concepts for apothecial fungi and has been bers. In a series of studies, we contributed to the enumeration of used since the establishment of Helotiales by Nannfeldt (1932). In undocumented taxa, including new species (Hosoya & Otani, his taxonomy, Helotiales were divided into eight families (Ascocor- 1997a, 1997b; Hosoya & Harada, 1999; Ono & Hosoya 2001; Tanaka ticiaceae, Dermateaceae, Geoglossaceae, Hemiphacidiaceae, Hyalos- & Hosoya, 2001; Tochihara & Hosoya, 2019). cyphaceae, Leotiaceae, Orbiliaceae, and Sclerotiniaceae), whereas a Cantrell and Hanlin (1997) first conducted a phylogenetic anal- more recent treatment (Baral, 2016) recognized greater taxonomic ysis to assess the taxonomy of Hyaloscyphaceae using a single gene, diversity in 25 families (Table 1). Reviewing recent taxonomic stud- ITS-5.8S. In their analysis, they clarified most of the genera in ies in Japan based on the classification by Korf (1973), Ascocortici- Lachneae, which formed a monophyletic group, but the phylogeny aceae had not yet been documented. Geoglossaceae has been almost of higher clades was less supported. Hosoya et al. (2010c) conduct- completely unstudied since Imai (1934) and is now treated as an ed a multi-gene analysis using the combined data of ITS-5.8S, the independent class apart from Helotiales (Schoch et al., 2009). Orbil- D1-D2 region
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